Distinct modes of manipulation of rice auxin response factor OsARF17 by different plant RNA viruses for infection

Abstract

Plant auxin response factor (ARF) transcription factors are an important class of key transcriptional modulators in auxin signaling. Despite the well-studied roles of ARF transcription factors in plant growth and development, it is largely unknown whether, and how, ARF transcription factors may be involved in plant resistance to pathogens. We show here that two fijiviruses (double-stranded RNA viruses) utilize their proteins to disturb the dimerization of OsARF17 and repress its transcriptional activation ability, while a tenuivirus (negative-sense single-stranded RNA virus) directly interferes with the DNA binding activity of OsARF17. These interactions impair OsARF17-mediated antiviral defense. OsARF17 also confers resistance to a cytorhabdovirus and was directly targeted by one of the viral proteins. Thus, OsARF17 is the common target of several very different viruses. This suggests that OsARF17 plays a crucial role in plant defense against different types of plant viruses, and that these viruses use independently evolved viral proteins to target this key component of auxin signaling and facilitate infection.

Auxin response factors (ARFs) differentially regulate rice antiviral immune response against rice dwarf virus

“…Accumulating evidence suggests that many viruses maximize their multiplication through disrupting the host plant's auxin signaling [12,[27][28][29]. For example, Tobacco mosaic virus (TMV)'s replicase protein interacts with IAA26 protein, disrupting the localization and stability of IAA26 protein, causing altered auxin signaling and reduced disease resistance in the host plant [27,28].…”

“…For example, Tobacco mosaic virus (TMV)’s replicase protein interacts with IAA26 protein, disrupting the localization and stability of IAA26 protein, causing altered auxin signaling and reduced disease resistance in the host plant [ 27 , 28 ]. Several different plant RNA viruses manipulate rice auxin signaling by using independently evolved viral proteins to target OsARF17, the key component of auxin signaling pathway to facilitate infection [ 29 ]. We previously showed that stabilization or increased accumulation of OsIAA10 enhances rice susceptibility to RDV infection.…”

“…As a counter-defense, plant viruses also have evolved strategies to manipulate plant responses (such as plant's hormone responses) for their own benefit [4, 12-14, 18, 21-23]. For example, it has been shown that virus can modulate a number of plant hormone signaling pathways (such as gibberellin, ethylene and auxin) to counteract the host plant's defense responses [11][12][13][14][23][24][25][26][27][28][29]. Previous studies in our laboratory have shown that RDV-encoded Pns11 protein promotes ethylene production to enhance plant susceptibility to viral infection [13].…”

“…P2 also contributes to the dwarf phenotype of infected rice plants by interfering with auxin signaling through interacting with OsIAA10, thus enhancing viral infection and pathogenesis [ 12 ]. Most recently, it was reported that several different plant RNA viruses manipulate rice auxin signaling by targeting OsARF17, one of the components of auxin signaling pathway to facilitate infection [ 29 ]. These studies demonstrate the broad significance of viral inhibition or manipulation of multiple hormonal pathways to benefit infection and enhance disease symptoms [ 11 – 14 , 27 – 29 ].…”

“…Most recently, it was reported that several different plant RNA viruses manipulate rice auxin signaling by targeting OsARF17, one of the components of auxin signaling pathway to facilitate infection [ 29 ]. These studies demonstrate the broad significance of viral inhibition or manipulation of multiple hormonal pathways to benefit infection and enhance disease symptoms [ 11 – 14 , 27 – 29 ].…”